Involving community pharmacists in interprofessional collaboration in primary care: a systematic review

Background The World Health Organization supports interprofessional collaboration in primary care. On over the past 20 years, community pharmacists had been taking a growing number of new responsibilities and they are recognized as a core member of collaborative care teams as patient-centered care providers. This systematic review aimed to describe interprofessional collaboration in primary care involving a pharmacist, and its effect on patient related outcomes. Methods A systematic review of randomized controlled trials cited in the MEDLINE, EMBASE, PsycInfo and CINAHL in English and French was conducted from inception to November 2022. Studies were included if they described an intervention piloted by a primary care provider and included a pharmacist and if they evaluated the effects of intervention on a disease or on patient related outcomes. The search generated 3494 articles. After duplicates were removed and titles and abstracts screened for inclusion, 344 articles remained. Results Overall, 19 studies were included in the review and assessed for quality. We found 14 studies describing an exclusive collaboration between physician and pharmacist with for all studies a three-step model of pharmacist intervention: a medication review, an interview with the patient, and recommendations made to physician. Major topics in the articles eligible for inclusion included cardiovascular diseases with blood pressure, diabetes, dyslipidemia, and risk of cardiovascular diseases. Positive effects concerned principally blood pressure. Conclusions Collaboration involving pharmacists is mainly described in relation to cardiovascular diseases, for which patient-centered indicators are most often positive. It underscores the need for further controlled studies on pharmacist-involved interprofessional collaboration across various medical conditions to improve consensus on core outcomes measures. Supplementary Information The online version contains supplementary material available at 10.1186/s12875-024-02326-3.


Introduction
The World Health Organization supports interprofessional collaboration in primary care [1].Interprofessional collaboration is defined as multiple health professionals from different backgrounds working together with patients, their families, carers and communities to deliver high quality patient-centered care [1].In primary care, interprofessional collaboration has been shown to improve patient pathways, healthcare efficiency and costeffectiveness [2][3][4], and job satisfaction for healthcare providers [5,6].
Delegating healthcare responsibilities to pharmacists in the context of interprofessional collaboration is one aspect of healthcare that has been adapted to meet the increasing demands and needs to access safe and effective healthcare [5,7].This became particularly necessary during the COVID-19 pandemic when interprofessional collaboration rapidly developed to support severely challenged healthcare systems worldwide [8].To address the heightened strain on healthcare resources, several countries have restructured emergency medical services and reassigned healthcare professional responsibilities [9].This includes the participation of community pharmacists in COVID-19 screening and vaccination [10,11].These additional responsibilities further expanded the growing number of new responsibilities that pharmacists had been taking on over the past 20 years.They include screening for human immunodeficiency virus (HIV) [12], diabetes [13], or cancer [14,15], prescribing medication (initiation, continuation or modification) [16][17][18] and reviewing and monitoring prescribing guidelines [19].
To date, some reviews have investigated interprofessional collaborations in healthcare [20,21].However, little information is available in the literature about the effects of pharmacist involvement in interprofessional collaboration in primary care, and how it is organized.This systematic review aimed to describe interprofessional collaboration in primary care involving a pharmacist, and its effect on disease or patient related outcome.

Method
This systematic review was performed according to PRISMA guidelines [22], using MEDLINE (Pubmed), EMBASE, PsycInfo and CINAHL from inception to July 2021.Subsequently, an abbreviated MEDLINE search update from July 2021 to November 2022 was performed.This review constitutes a secondary analysis of a systematic review conducted on interprofessional collaborations in primary care [23].
The following search strategy was used in PubMed: ("Intersectoral Collaboration"[Mesh] OR "Cooperative Behavior"[Mesh] OR "Patient Care Team"[Mesh:NoExp]) AND ("Primary Health Care"[Mesh]) AND ("Outcome and Process Assessment, Health Care" [Mesh])."This search strategy was adapted to the syntax of Embase, PsychINFO, and CINHAL databases: "intersectoral collaboration", "cooperative behavior", "patient care team" AND "primary health care" AND "outcome and process assessment, health care".The details concerning the search strategy were presented in Supplementary material 1.
To be included, a study had to have reported a randomized controlled trial (RCT) evaluating the effects of a pharmacist intervention on a disease or patient related outcome.The intervention had to be in the context of interprofessional collaboration, which was piloted by a primary care provider and published in English or French.Studies were excluded if they did not report interprofessional collaboration and if they were not in IMRAD format.
Four reviewers (SG, LR, AN and AM) screened the titles and abstracts of the database records and retrieved the full texts and independently examined the studies for eligibility.Disagreements were resolved by consensus discussion with three reviewers (MJ, MA, JFH).The reference lists of included studies were hand searched for additional citations.In a second stage, given the large number of articles, only articles involving a pharmacist were selected.
From those studies included, data concerning the study (authors, publication date, country, sample size, objective and pathology, study duration, inclusion criteria), the intervention (professionals involved, intervention type or practice collaboration), and measures to assess the intervention effect (main outcome measure, secondary outcomes) were extracted.
Two independent reviewers (MA, JFH) appraised the risk of bias and quality of each included study using the Integrated Quality Criteria for Review of Multiple Study Designs (ICROMS) tool [24].
The systematic review was registered in PROSPERO under number CRD42021278461.The registered protocol substantially differs from the review methods.We have focused on pharmacist interventions and presented only results on the effects of interprofessional collaboration on patients to enhance clarity.We have increased reviewers from two to four to address the paper volume."

Results
Figure 1 presents the PRISMA Flow Diagram.In total, 3472 records were identified of which 2242 were excluded.The excluded studies were interventions delivered by a secondary care professional or did not investigate interprofessional collaboration.Then, 1230 abstracts and 344 full text papers were screened for eligibility and 19 were included in the review.

Characteristics of pharmacist intervention
Supplementary material 2 lists the characteristics of pharmacist intervention.Most studies investigated a collaborative intervention involving only a physician and a pharmacist [25-29, 32, 33, 35-38, 41-43].Two studies  To study whether a home-based intervention in an at-risk elderly population could reduce hospital admissions Table 1 Characteristics of included studies involved a physician, a pharmacist, and a nurse [30,31].Three studies involved a pharmacist and an allied health team consisting of physicians, nurses, dietitians, psychotherapists, care managers, social workers or psychiatrists [34,39,40].Overall, the pharmacist intervention typically involved medication review, patient interviews, and recommendations to physicians.The medication review was performed using data recorded in an electronic medical record database, then completed with a telephone or face-to-face patient interview [26, 34-36, 38, 39, 43].One study involved nurses who developed an individualized care plan with the patient and in consultation with the pharmacist and the physician [30].The frequency of clinical contact with patients varied from 2 [41,43] to 12 or more contacts [27].The physician was free to accept or reject pharmacist recommendations except in one study where the pharmacist had the authorization to directly modify medications, and the physician was solely informed [29].In all the other studies, recommendations to physicians were provided either during face-to-face contact [25,26,28,37,[41][42][43], or by telephone [37,40,42] or email [26,27,29,33,35,39,42,43]. The acceptance rate for pharmacist interventions was reported in seven studies and was between 76.6% and 96.2% [25,27,28,33,36,38,43].
However, three studies, also assessed additional activities combined with the typical pharmacist intervention.Heisler et al. (2012), investigated an intervention in which the pharmacist suggested and prescribed treatment changes directly to the patient [29].Three studies investigated a pharmacist intervention that involved taking clinical measurements (blood pressure, heart rate or weight) and laboratory tests [25,29,34].In all studies, participants in the control group did not benefit from pharmacist intervention; instead, they were exclusively received usual care from physicians alone [25-29, 31, 33, 35-38, 40, 41, 43] or from primary care teams composed on physicians and nurses [30,32,34,39,42].
Table 2 lists the outcome measures and significant results studied for the various pathologies.We found that the effect of pharmacist intervention varied depending on the outcome measure and follow-up duration.In supplementary material 3, a table lists the outcome measures and significant and non-significant results.
Concerning blood pressure reduction, most studies reported that the pharmacist intervention significantly lowered blood pressure [25,26,28,34,35,37,38] with a follow-up duration ranging from 6 to 12 months.Four studies did not report any effect [27,29,30,33].Concerning blood pressure control, defined as blood pressure measured lower than 130/80 mmHg for patients with diabetes mellitus or chronic disease and lower than 140/90 for all other patients, two studies found pharmacist intervention had a positive effect [25,28] and four studies did not find any effect [26,27,35,37].
Concerning pharmacist interventions to reduce cardiovascular diseases and risk factors, Simpson et al. ( 2011) reported a significant reduction of 1.5% (95% CI -0.2 to 3.3) in predicted 10-year cardiovascular event risk [34].More specifically, Tobari et al. (2010) reported lower Body Mass Index (BMI), sodium score and fewer smokers, but no effect was demonstrated among patients with alcohol consumption > 23 g/day or with brisk walking > 30 min/day [37].
Two studies focused on depressive disorders with one showing that patients expressed greater satisfaction than controls with a pharmacist intervention but neither reported an effect of pharmacist intervention on patient related outcome [40,42].
Five studies evaluated medication adherence [25,32,35,39,40], two of which reported a positive effect of   pharmacist intervention on patient adherence to medication, including a post-hoc analysis among an ethnic minority group [35,39].Three studies did not report significant results [25,32,40].None of the three studies identified demonstrated an effect of pharmacist intervention on the quality of life in older people [30,41,43].
For the studies evaluating the pharmacist role in preventative medicine, a positive effect was observed for influenza vaccination, colorectal cancer screening, hearing and eye examination [30], BMI screening and follow-up and alcohol use [27].However, no effect was observed on breast and cervical cancer screening [30], diabetic foot examination, dilated eye examination, microalbumin measurement and proportion of smokers advised to quit [27].Pape et al. (2011) found that a higher proportion of patients underwent a LDL-C test in the intervention group [33].
Lastly, a positive effect of pharmacist intervention was observed in an interprofessional collaboration.Patients appreciated the personal nature of care, provider availability, provider ability to listen, explanation of why antidepressants were prescribed, and the explanation of how to take the antidepressants and, overall, patients were satisfied with the pharmacist intervention [39,40].Pape et al. (2011) did not find significant results [33].
Fig. 3 provides a synthesized overview of the evidence pertaining on interprofessional collaboration

Critical appraisal of studies
According to the ICROMS quality assessment, six studies had a low risk of bias [30,31,33,34,37,41], meeting both minimum score and mandatory criteria .Nine studies had a moderate risk of bias; minimum ICROMS scores were met but mandatory scores were not [25-29, 35, 38, 40, 43].The remaining four studies had a high risk of bias, with neither minimum or mandatory scores being met [32,36,39,42].The results are summarized in Table 3.

Discussion
This systematic review identified 19 randomized controlled trials evaluating the effects of pharmacist interventions in primary care conducted in various countries and different health care settings.Most studies concerned a physician-pharmacist collaboration and only five studies included a physician and other health professionals.All studies included a standard pharmacist intervention involving medication review, patient interview, and recommendations to the physician.However, three studies also included additional responsibilities.Interestingly we found an over-representation of RCTs among patients with cardiovascular risk factors such as hypertension, diabetes, or dyslipidemia.Only six studies evaluated pharmacist involvement in interprofessional collaboration among patients with other pathologies and with mixed results.
The standard pharmacist intervention involving medication review, patient interview, and recommendations to the physician is in accordance with previously described literature [44,45].However, some studies also included Fig. 3  Table 3 Risk of bias assessment using ICROMS additional responsibilities in the intervention including new medicine prescription, laboratory assessments or deprescribing which is also consistent with existing literature [44,46].The additional responsibilities identified in our review should be compared with the roles assigned to community pharmacists in different countries.Notably, the implementation of legislation supporting pharmacist prescribing in the United Kingdom, Canada, the United States, and New Zealand may explain the emergence of these new responsibilities highlighted in our review [47,48].In this collaboration, physicians were also core members.Previous authors have analyzed pharmacistphysician collaboration [45,49,50], either to determine factors influencing collaboration [51] or to explore attitudes towards interprofessional collaboration [52].Only five studies involved other health professionals, which was less than expected.Because of the limited number of studies incorporating more than two professionals, we were unable to investigate the correlation between the number of professions in a collaboration and its impact on patient health and satisfaction outcomes.However, this variable was explored in a recent systematic review which found no association between the number of professions in the interprofessional collaboration and HbA1c reduction [53].
A large majority of included articles evaluated the role of a pharmacist intervention in managing cardiovascular diseases and risk factors, particularly blood pressure.This supports evidence from recent reviews [44,53,54].Indeed, the meta-analysis of Tan et al. (2014), including four studies that were also included in our review [29,30,34,37], reported that interventions involving pharmacists or nurses were associated with significantly improved BP control [44].Moreover, some included studies reported that pharmacist care improved lipid parameters, notably LDL-C levels, as well as increasing the proportion of patients who achieved targeted levels which is consistent with existing literature [55].In contrast, results concerning HbA1c were conflicting.Whilst we found only one study reporting positive effects, previous research reported more studies with positive effects on HbA1c with pharmacist interventions [44,56,57].Tan et al. (2014) found four studies with positive effects and two studies with no effect and concluded with a metaanalysis that HbA1c reduced by 0.88% in the intervention group [44].In Pousinho et al. (2016) review, HbA1c was considered as an outcome measure in 26 studies and 24 studies reported a greater improvement in this outcome in the intervention group compared with the control group [56].The divergence in results could be explained by the fact that in our included studies, the pharmacist interventions were not directly focused on diabetes but were a secondary outcome measure.
Concerning quality of life and patient satisfaction, our review did not report significant results.Many different assessment tools were used to explore these two variables which may explain these results.Similarly, an umbrella review conducted by Abdulrhim et al. (2020) was unable to conclude about improvements in quality of life for patients with diabetes due to the use of diverse quality of life assessment tools [57].

Bias of included studies
Only randomized controlled trials were included in this systematic review because they provide the most reliable evidence on intervention effectiveness.However, the quality assessment revealed that the majority of the included studies had a moderate risk of bias mainly due to their methodological quality.No article had a methodology with double blinding, which is a strong criterion in quality assessment.This absence was anticipated, considering the nature of the interventions, where professionals involvement precludes blinding.Therefore, the certainty of evidence supporting the conclusions about intervention effectiveness is low.

Limitations
Despite following PRISMA guidelines, our systematic review did have some limitations.Firstly, the exclusive focus on RCTs improves the robustness of the review.However, there is limited availability of relevant RCTs for significant primary care topics, such as chronic  obstructive pulmonary disease [58], or infection [59], which were consequently omitted from our synthesis.Secondly, even though we chose to only include RCTs, it was still difficult to group the outcomes to assess the effect of pharmacist involvement in a primary care interprofessional team.A number of factors explain this, including the differences in patient populations, followup durations, instruments used to measure outcome and intervention complexity.These discrepancies deserve further thought and investigation into appropriate core outcome measure to be used in primary care research and strategies and methods currently used to optimize implementation of complex interventions [60,61].Thirdly, the quality assessment revealed that the majority of included studies had a moderate risk of bias due to their methodological quality.Finally, there is no existing consensus defining interprofessional collaboration [62,63] and the search strategy had to consider several terms.We used Mesh terms in the search strategy to be more specific.Moreover, to our knowledge, there are no recommendations about professions which should be involved in a primary care interprofessional team, and this made it difficult to select studies.

Conclusion
This review revealed that pharmacists are mainly responsible for medication review, interview with patients and recommendations to physicians, and most commonly collaborate with physicians.Pharmacist collaboration particularly improved blood pressure and cholesterol control.Our review highlights the need for further controlled studies into interprofessional collaboration interventions involving a pharmacist in primary care across the full range of medical conditions.

Fig. 2
Fig. 2 Illustration of Investigated Topic Frequencies in Selected Studies.Legend: the bigger the circle, the more studied the topic.Abbreviations: CV risk: cardiovascular risk

Table 2
Summary of outcomes with significant results : Synthesis of the impact of interprofessional collaboration categorized by subject.Abbreviations: CV risk: cardiovascular risk